The OsbZIP23 transcription factor has been characterized for its essential role in drought resistance in rice (Oryza sativa), but the mechanism is unknown. In this study, we first investigated the transcriptional activation of OsbZIP23. A homolog of SnRK2 protein kinase (SAPK2) was found to interact with and phosphorylate OsbZIP23 for its transcriptional activation. SAPK2 also interacted with OsPP2C49, an ABI1 homolog, which deactivated the SAPK2 to inhibit the transcriptional activation activity of OsbZIP23. Next, we performed genome-wide identification of OsbZIP23 targets by immunoprecipitation sequencing and RNA sequencing analyses in the OsbZIP23-overexpression, osbzip23 mutant, and wild-type rice under normal and drought stress conditions. OsbZIP23 directly regulates a large number of reported genes that function in stress response, hormone signaling, and developmental processes. Among these targets, we found that OsbZIP23 could positively regulate OsPP2C49, and overexpression of OsPP2C49 in rice resulted in significantly decreased sensitivity of the abscisic acid (ABA) response and rapid dehydration. Moreover, OsNCED4 (9-cis-epoxycarotenoid dioxygenase4), a key gene in ABA biosynthesis, was also positively regulated by OsbZIP23. Together, our results suggest that OsbZIP23 acts as a central regulator in ABA signaling and biosynthesis, and drought resistance in rice.
Abiotic stresses such as drought cause a reduction of plant growth and loss of crop yield. Stomatal aperture controls CO2 uptake and water loss to the atmosphere, thus playing important roles in both the yield gain and drought tolerance of crops. Here, a rice homologue of SRO (similar to RCD one), termed OsSRO1c, was identified as a direct target gene of SNAC1 (stress-responsive NAC 1) involved in the regulation of stomatal aperture and oxidative response. SNAC1 could bind to the promoter of OsSRO1c and activate the expression of OsSRO1c. OsSRO1c was induced in guard cells by drought stress. The loss-of-function mutant of OsSRO1c showed increased stomatal aperture and sensitivity to drought, and faster water loss compared with the wild-type plant, whereas OsSRO1c overexpression led to decreased stomatal aperture and reduced water loss. Interestingly, OsSRO1c-overexpressing rice showed increased sensitivity to oxidative stress. Expression of DST, a reported zinc finger gene negatively regulating H2O2-induced stomatal closure, and the activity of H2O2-scavenging related enzymes were significantly suppressed, and H2O2 in guard cells was accumulated in the overexpression lines. OsSRO1c interacted with various stress-related regulatory and functional proteins, and some of the OsSRO1c-interacting proteins are predicted to be involved in the control of stomatal aperture and oxidative stress tolerance. The results suggest that OsSRO1c has dual roles in drought and oxidative stress tolerance of rice by promoting stomatal closure and H2O2 accumulation through a novel pathway involving regulators SNAC1 and DST.
Histone modifications affect gene expression level. Several studies have shown that they may play key roles in regulating gene expression in plants under abiotic stress, but genome-wide surveys of such stress-related modifications are very limited, especially for crops. By using ChIP-Seq and RNA-Seq, we investigated the genome-wide distribution pattern of histone H3 lysine4 tri-methylation (H3K4me3) and the pattern's association with whole genome expression profiles of rice (Oryza sativa L.) under drought stress, one of the major and representative abiotic stresses. We detected 51.1 and 48 % of annotated genes with H3K4me3 modification in rice seedlings under normal growth (control) and drought stress conditions, respectively. By RNA-Seq, 76.7 and 79 % of annotated genes were detected with expression in rice seedlings under the control and drought stress conditions, respectively. Furthermore, 4,837 genes were differentially H3K4me3-modified (H3M), (3,927 genes with increased H3M; 910 genes with decreased H3M) and 5,866 genes were differentially expressed (2,145 up-regulated; 3,721 down-regulated) in drought stress. Differential H3K4me3 methylation only affects a small proportion of stress-responsive genes, and the H3K4me3 modification level was significantly and positively correlated with transcript level only for a subset of genes showing changes both in modification and expression with drought stress. Moreover, for the H3K4me3-regulated stress-related genes, the H3K4me3 modification level was mainly increased in genes with low expression and decreased in genes with high expression under drought stress. The comprehensive data of H3K4me3 and gene expression profiles in rice under drought stress provide a useful resource for future epigenomic regulation studies in plants under abiotic stresses.
Plants have evolved complicated protective mechanisms to survive adverse conditions. Previously, we reported that the transcription factor OsbZIP46 regulates abscisic acid (ABA) signaling-mediated drought tolerance in rice () by modulating stress-related genes. An intrinsic D domain represses OsbZIP46 activity, but the detailed mechanism for the repression of OsbZIP46 activation remains unknown. Here, we report an OsbZIP46-interacting protein, MODD (Mediator of OsbZIP46 deactivation and degradation), which is homologous to the ABSCISIC ACID-INSENSITIVE5 binding protein AFP. was induced by ABA and drought stress, but the induction was much slower than that of In contrast to OsbZIP46, MODD negatively regulates ABA signaling and drought tolerance, and inhibits the expression of OsbZIP46 target genes. We found that MODD negatively regulates OsbZIP46 activity and stability. MODD represses OsbZIP46 activity via interaction with the OsTPR3-HDA702 corepressor complex and downregulation of the histone acetylation level at OsbZIP46 target genes. MODD promotes OsbZIP46 degradation via interaction with the U-box type ubiquitin E3 ligase OsPUB70. Interestingly, the D domain is required for both deactivation and degradation of OsbZIP46 via its interaction with MODD. These findings show that plants fine-tune their drought responses by elaborate regulatory mechanisms, including the coordination of activity and stability of key transcription factors.
Plants respond to abiotic stresses through a complexity of signaling pathways, and the dephosphorylation mediated by protein phosphatase (PP) is an important event in this process. We identified a rice (Oryza sativa) PP2C gene, OsPP18, as a STRESS-RESPONSIVE NAC1 (SNAC1)-regulated downstream gene. The ospp18 mutant was more sensitive than wild-type plants to drought stress at both the seedling and panicle development stages. Rice plants with OsPP18 suppressed through artificial microRNA were also hypersensitive to drought stress. Microarray analysis of the mutant revealed that genes encoding reactive oxygen species (ROS) scavenging enzymes were down-regulated in the ospp18 mutant, and the mutant exhibited reduced activities of ROS scavenging enzymes and increased sensitivity to oxidative stresses. Overexpression of OsPP18 in rice led to enhanced osmotic and oxidative stress tolerance. The expression of OsPP18 was induced by drought stress but not induced by abscisic acid (ABA). Although OsPP18 is a typical PP2C with enzymatic activity, it did not interact with SNF1-RELATED PROTEIN KINASE2 protein kinases, which function in ABA signaling. Meanwhile, the expression of ABA-responsive genes was not affected in the ospp18 mutant, and the ABA sensitivities of the ospp18 mutant and OsPP18-overexpressing plants were also not altered. Together, these findings suggest that OsPP18 is a unique PP2C gene that is regulated by SNAC1 and confers drought and oxidative stress tolerance by regulating ROS homeostasis through ABA-independent pathways.
SIMILAR TO RCD ONE (SRO) is a plant-specific gene family involved in development and abiotic stress responses. SRO proteins are characterized by containing poly (ADP-ribose) polymerase catalytic (PARP) and C-terminal RCD1-SRO-TAF4 domains, and can be classified into two groups and five subgroups on the basis of their PARP domain. Expression analysis of rice SRO genes in response to various abiotic stresses showed that OsSRO1c, a rice SRO gene which functions downstream of the stress-responsive transcription factor SNAC1, is the major stress-responsive gene in the rice SRO family. The ossro1c-1 mutant showed resistance not only to chloroplastic oxidative stress, but also to apoplastic oxidative stress. However, the ossro1c-1 mutant and artificial microRNA-OsSRO1c transgenic rice were significantly impaired in cold tolerance. When compared with the well-characterized Arabidopsis SRO protein radical-induced cell death 1 (RCD1), OsSRO1c has considerable variation in the protein sequence, and the two genes exhibit different expression profiles under abiotic stresses. Furthermore, ossro1c-1 and rcd1 showed different responses to multiple abiotic stresses. By screening an Arabidopsis transcription factor library, 29 transcription factors interacted with OsSRO1c in yeast, but only two of these transcription factors were reported to interact with RCD1, which may partly explain the different responses of the two mutants under various stresses. The data presented in this report provide important clues for further elucidating the molecular and biochemical mechanisms of OsSRO1c in mediating responses to multiple abiotic stresses.
Thousands of differentially expressed genes (DEGs) have been identified in rice under drought stress conditions. However, the regulatory mechanism of these DEGs remains largely unclear. Here, we report an interplay between histone H3K4me3 modification and transcription factor OsbZIP23 in the regulation of a dehydrin gene cluster under drought stress conditions in rice. When the H3K4me3 modification level was increased, the dehydrin gene expression levels were increased, and the binding levels of OsbZIP23 to the promoter of the dehydrin genes were also enhanced. Conversely, the H3K4me3 modification and dehydrin gene expression levels were downregulated in the osbzip23 mutant under drought stress conditions. Our study uncovers a collaboration between transcription factor and H3K4me3 modification in the regulation of droughtresponsive genes, which will help us to further understand the gene regulation mechanism under stress conditions in plants.
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